Relations Between Sleep and Temperament in Preschool Children With ADHD

Abstract

Objective: The objective of this study was to assess the links between temperament and sleep in a group of preschoolers with ADHD. Method: Twenty-five ADHD (M = 5.37 years, SD = 1.09) and 22 typically developing (TD; M = 5.10, SD = 1.18) preschoolers participated in the study. Sleep was assessed with the Sleep Disturbance Scale and wrist actigraphy. The Preschool Temperament and Character Inventory (PsTCI) was used to evaluate the child temperament. Results: ADHD children showed a temperamental profile characterized by higher novelty seeking, lower persistence, self-directness, and cooperativeness and marginally lower harm avoidance (HA) compared with controls. HA was associated negatively to wakefulness after sleep onset and sleep fragmentation and positively with sleep efficiency and sleep time. Reward dependence was negatively associated with wake episode length. Conclusion: Sleep and temperament are correlated in preschoolers with ADHD and temperament might represent an intermediate endophenotype underlying the relation between ADHD and sleep disorders.

Keywords

temperament ADHD sleep actigraphy preschool children

Introduction

The relation between sleep–wake regulation and ADHD is still a debated matter. Parental report of sleep disturbances in children with ADHD shows a high prevalence of bedtime struggles, difficulty falling asleep, night awakenings, and movements during sleep, versus a nonclinical population (Corkum, Tannock, & Moldofsky, 1998; Gruber, 2009; Owens et al., 2009; Van der Heijden, Smits, Van Someren, Ridderinkhof, & Gunning, 2007). When objectively evaluated, however, few differences have been found between ADHD and controls in polysomnographic (PSG) and actigraphic parameters (Corkum, Tannock, Moldofsky, Hogg-Johnson, & Humphries, 2001; Hvolby, Jorgensen, & Bilenberg, 2008; Owens et al., 2009; Sadeh, Pergamin, & Bar-Haim, 2006).

To explain the nature of the relation between ADHD and sleep problems, other components of the child development should be analyzed. Because temperament is considered to be a determinant factor for the regulation of arousal, emotion, and behavior, its influence on the sleep development could play a role in explaining the underlying mechanisms linking sleep and ADHD.

The relation between temperament and sleep patterns, sleep quality, and their variability during the first year of life (for a review, see Ednick et al., 2009) might stem from an underlying physiological reactivity factor (Carey, 1974) because they share a strong biological basis (Raizen, Mason, & Pack, 2006; Rothbart & Bates, 2006). Conversely, sleep fragmentation might impair emotional and cognitive regulation, causing hypervigilance, distractibility, and other characteristics of difficult temperament, while parental styles in limit setting might influence sleep problems and the behavior characteristics of difficult temperament (Sadeh, Lavie, & Scher, 1994).

Empirical evidence has been reported that temperamental dimensions, such as rhythmicity, state regulations, activity level, irritability, and soothability, might be one set of contributors to the consolidation and characteristics of the child sleep (Carey & McDevitt, 1978; Keener, Zeanah, & Anders, 1988). Infants with positive mood, high approach, and sociability have been found to sleep longer at night or have fewer sleep problems than infants characterized by negative mood, high withdrawal, and poor regulatory capacity (Scher, Tirosh, & Lavie, 1998; Spruyt et al., 2008; Weissbluth, 1981). At the same time, a higher quality of infant/toddler sleep is strongly associated to higher persistence, adaptability, soothability, and lower distractibility (Kelmanson, 2004; Kiff, Lengua, & Zalewski, 2011; Scher et al., 1998).

In parallel, infants with a difficult temperament (defined as excessively emotionally negative and persistent/unstoppable, low adaptable) sleep less and have more bedtime resistance, lower rhythmicity, adaptability and approach (Bruni et al., 2006; Owens-Stively et al., 1997), higher reactivity, and low regulation (Goodnight, Bates, Staples, Pettit, & Dodge, 2007) than the so-called “easy” babies. Furthermore, difficult temperament in infancy has been related to behavioral and sleep disturbances in childhood (Zuckerman, Stevenson, & Bailey, 1987). Other studies reported that infants with high-activity level show more variability in nighttime sleep than infants with low-activity level, as well as high-negative mood associated to short sleep duration (Kelmanson, 2004; Kiff et al., 2011).

Notwithstanding the strict correlation between sleep and temperament, research has been limited to infants and toddlers and with the almost exclusive use of sleep measures based on parental reports. The few studies that have assessed sleep and temperament, using sleep diaries and actigraphy, at several time points during the first year of life, confirmed that good sleep is correlated with an “easy” temperament characterized by high approachability, rhythmicity, adaptability, and low distractibility (Spruyt et al., 2008).

However, most of the studies have been conducted in the general population and not in well-defined clinical population. In particular, to our knowledge, no studies have assessed the relationship between sleep and temperament in children with ADHD using objective measures. Because actigraphy allows an objective assessment and a valid procedure to discriminate between sleep-disturbed subjects and good sleepers (Sadeh, Lavie, Scher, Tirosh, & Epstein, 1991), the aim of this study was to examine (a) the temperamental profiles in preschoolers with ADHD compared with that of typically developing (TD) children; and (b) the relations between temperament and sleep characteristics in preschool children with ADHD, using both actigraphic measures and parental reports.

Method

Participants

Participants were 25 ADHD preschoolers (21 males, 84%; mean age = 5.37 years; SD = 1.09; range = 4-6 years) recruited from the Child and Adolescent Neuropsychiatry Outpatient Center, Rome (Italy). Children with positive neurological examination or electroencephalographic (EEG) abnormalities, sensory-motor deficits, cognitive impairment (IQ < 70) evaluated with the Wechsler Intelligence Scale for Children–III (WISC-III), or autistic disorder were excluded from the study. For the diagnosis of ADHD and comorbidity disorders, we used the Preschool Age Psychiatric Assessment (PAPA) interview to parents (Egger et al., 2006), based on Diagnostic and Statistical Manual of Mental Disorders (4th ed.; DSM-IV; American Psychiatric Association, 1994) criteria, supported by behavioral observation. Among these children, six of them (24%) were diagnosed with the inattentive subtype, nine (36%) with the hyperactive–impulsive subtype, and 10 (40%) with the combined subtype. Regarding psychiatric comorbidity, oppositional defiant disorder was found in 10 cases (40%), generalized anxiety disorder in three cases (12%), and depression in two cases (8%).

For the present study, we also considered 22 TD preschool children (14 males, 64%; mean age = 5.10 years, SD = 1.18; range = 4-6 years) recruited in a day care center located in Rome (Italy). The two groups were composed of Caucasian children. Informed parental consent was obtained for all participants (100%). The study was approved by the institutional review board.

Procedure

The data reported here are part of a larger study designed to investigate sleep and temperament in ADHD preschool children. Details about samples, methodology, actigraphic procedures, and measures utilized and the Temperament and Character Inventory (TCI) version for preschooler (PsTCI) Italian validation have been previously described in separate studies (Melegari, Innocenzi, Marano, Donfrancesco, & Cloninger, 2014; Melegari et al., 2015; Melegari et al., 2018).

For both groups, actigraphs were provided to the parents (or caregivers) with the information regarding its use. In children with intercurrent diseases, the actigraphic study was replicated when they were in a healthy condition. Parents completed the PsTCI and the sleep questionnaire. The PsTCI was analyzed by a certified child psychiatrist, with several years of expertise in its use.

Measures

Sleep questionnaire

To assess the presence or absence of sleep disorders, we used the adapted version of the Sleep Disturbance Scale for Children (SDSC; Bruni et al., 1996). The questionnaire is composed of 24 items on a 3-point Likert-type scale (0 = never; 1= sometimes or 1-2 times per week; 2 = more than 2 times per week). The questionnaire is divided into four sections: (a) bedtime; (b) behavior during sleep; (c) morning awakening; and (d) daytime somnolence. For the purpose of this study and according with previous studies (e.g., Melegari et al., 2018), the item scores were recoded based on a dichotomic scale (0 = absence, 1 or 2 = presence).

Actigraphy

Actigraphy is a simple method to objectively evaluate sleep patterns, consisting of a wrist-watch-sized activity sensor worn on the nondominant wrist, to discriminate between sleep–wake states through documentation of body movements. It is used in the child’s natural environment and allows for multiple-day data collection (Sadeh, Sharkey, & Carskadon, 1994). In the current study, we used the Watch-Motionloggers from Ambulatory Monitoring, Inc. (Ardsley, NY) to measure sleep parameters and nocturnal motor activity. These actigraphs employ a piezoelectric sensor, have a fixed sensitivity at 2 to 3 Hz, and detect accelerations greater than 0.01 g force. The mechanism is housed in a metal, waterproof case and has a 32K memory. The actigraphs were programmed to employ a zero-crossing mode using an auto actigraph interface.

Data were extracted using the ACT software and analyzed by means of the ACTIONW2 program, according to the validated sleep estimation algorithm developed by Sadeh et al. (1991).

Parents were instructed to allow the child to wear the watch continuously during the recording period except during baths or water play. During actigraphy data collection, parents were asked to keep their child’s regular sleep routine and record sleep–wake times. Moreover, parents were instructed to mark “lights out” and “get out of bed” events or when the actigraph was not worn by pressing the event marker of the actigraph.

For the present study, the following actigraphic data variables were considered: (a) Total Sleep Duration: the period of time in minutes from the marked “lights out” to the marked “get out of bed”; (b) Sleep Latency: minutes from the time the parents’ note of “lights out” to the first period of sleep lasting more than 20 min (sleep-onset); (c) Sleep Minutes: the period of sleep time in minutes from the sleep onset to morning awakening time minus the wake after sleep onset; (d) Wake After Sleep-Onset: the times in minutes of awakenings during the Sleep Minutes; (e) Mean Wake Episode: mean duration of wake episodes (minutes); (f) Sleep Efficiency: the ratio between the Sleep Minutes and the Total Sleep Duration × 100; (g) Activity Mean: the mean number of activity counts per 1-min epoch during Total Sleep Duration; (h) Activity Index (index of motor activity): the percent of epochs with >0 Activity Mean; and (i) Sleep Fragmentation Index: the ratio between the number of awakenings and the Sleep Minutes × 100.

In agreement with previous studies, intraindividual variability was calculated for each of the above parameters by calculating the within-subjects standard deviation of each variable (Gruber & Sadeh, 2004; Gruber, Sadeh, & Raviv, 2000; Moreau, Rouleau, & Morin, 2014).

Preschool Temperament and Character Inventory (PsTCI)

The PsTCI is a tool completed by parents to study the seven dimensions of personality of the Cloninger’s biosocial model (Costantino, Cloninger, Clarke, Hashemi, & Przybeck, 2002; for the Italian validation, see Melegari et al., 2014). The questionnaire is composed of 74 items on a 5-point Likert-type scale (1 = definitely false; 5 = definitely true). The contents of the items of each dimension were adapted to the age of preschool children and resulted to be unambiguous for parents.

The seven dimensions of the Cloninger’s model are divided into four temperament dimensions and three character dimensions. The temperament dimensions are (a) Harm Avoidance (HA) that represents the tendency to intensely respond to signals of adversative stimuli with inhibitory behaviors so as to avoid punishments, novelties, and frustrating nonrewards; (b) Novelty seeking (NS) that represents the tendency to respond with exhilaration and excitement to novel stimuli or cues for potential rewards, which leads to frequent exploratory activities in pursuing potential rewards as well as an active avoidance of monotony; (c) Reward Dependence (RD) that represents the tendency to intensely respond to signals of reward, in particular verbal signals of social approval; and (d) Persistence (PS) that represents a tendency to maintain or resist the extinction of behaviors that have previously been associated with rewards or relief from punishment (Cloninger, 1987; Cloninger, 2006).

The three character dimensions refer to individual differences in personal goals and values. The character dimensions are the following: (a) Self-Directness (SD) or the ability to self-regulate own behavior according to specific personal goals; (b) Cooperativeness (CO) that is the ability to develop the social learning defined by the maturation on interpersonal behavior as to be tolerant and empathic; (c) Self-Transcendence (ST) or the ability to well-being with nature and world and to go over individual experience that in preschoolers is represented by the capacity to pretend in play (Cloninger, Przybeck, Svrakic, & Wetzel, 1994).

Plan of Analyses

Data were first checked for their normality (i.e., skewness, kurtosis). Analyses of variance (ANOVAs) were conducted to analyze differences in temperament and character dimensions between ADHD and control groups. Pearson correlations and point biserial correlations (these last have been conducted between a categorical variable and a continuous variable) were performed in ADHD children to examine the associations between temperament and character dimensions, actigraphic sleep pattern, and sleep questionnaire. All the analyses were ran using the software SPSS for Windows Version 18.0 (IBM Corp., Armonk, NY).

Results

Findings from preliminary analyses revealed that none of variables had deviations from normality (values less than ǀ2ǀ for skewness and ǀ7ǀ for kurtosis).

There were no significant differences between children with ADHD and controls for age, F(1, 45) = 0.653), p = .42, and gender, χ²(1) = 2.552, p = .11.

Differences in Temperamental Dimensions Between ADHD and TD Groups

Descriptive statistics (means and standard deviations) for ADHD and control groups are reported in Table 1. Results of the ANOVAs indicated differences between the two groups on NS, PS, SD, CO, and HA (although this last was marginally significant). More specifically, compared with the control group, the ADHD group obtained lower scores in PS, SD, CO, and HA. In contrast, the ADHD group was perceived as more novelty seeker than the control group. No significant differences emerged between the two groups on RD and ST.

Table 1.

Comparison of Temperamental Characteristics in ADHD and Typically Developing Children.

	ADHD	Control	F	P	Partial η²
	M ± SD	M ± SD	F	P	Partial η²
Harm avoidance (HA)	2.30 ± 0.54	2.59 ± 0.53	3.246	< .10	0.07
Novelty seeking (NS)	3.53 ± 0.63	2.23 ± 0.51	59.470	<. 001	0.57
Reward dependence (RD)	4.04 ± 0.68	4.17 ± 0.43	0.576	.45	0.01
Persistence (PS)	2.34 ± 0.61	3.42 ± 0.60	37.075	<. 001	0.45
Self-directness (SD)	3.64 ± 0.64	4.00 ± 0.49	4.555	< .05	0.09
Cooperativeness (CO)	2.88 ± 0.73	4.10 ± 0.46	44.776	<. 001	0.50
Self-transcendence (ST)	3.44 ± 0.75	3.65 ± 0.64	1.043	.31	0.02

Correlations Between Temperamental Dimensions and Actigraphic Variables in ADHD Group

Correlations between temperamental dimensions and actigraphic sleep parameters (i.e., means, standard deviations) for the ADHD group are presented in Table 2. HA was positively associated with sleep minutes and sleep efficiency, negatively related to wake after sleep onset and sleep fragmentation index, and marginally negatively correlated with activity mean and activity index. NS was negatively associated with total sleep duration (although marginally), whereas RD was marginally and positively correlated with total sleep duration and significantly and negatively correlated with mean wake episodes. No other significant correlations emerged between temperament and character dimensions and mean actigraphic sleep parameters.

Table 2.

Bivariate Correlations Between Actigraphy Parameters (Mean and SD) and Temperament and Character Dimensions in Children With ADHD.

	Harm Avoidance (HA)	Novelty Seeking (NS)	Reward Dependence (RD)	Persistence (PS)	Self-Directness (SD)	Cooperativeness (CO)	Self-Transcendence (ST)
M
Total sleep duration	.22	−.35†	.34†	.13	.16	.25	−.14
Sleep latency	−.14	−.14	−.05	.02	.13	.23	.04
Sleep minutes	.45*	−.16	.33	.03	−.02	.11	−.01
Wake after sleep onset	−.53**	−.10	−.24	.09	.15	−.03	−.25
Mean wake episodes	−.25	.02	−.42*	−.13	−.13	−.17	−.32
Sleep efficiency	.50**	.02	.33	−.06	−.08	.07	.22
Activity mean	−.39†	−.01	−.29	.05	−.02	−.06	−.14
Activity index	−.38†	−.06	−.29	.13	.07	−.08	−.29
Sleep fragmentation index	−.50**	−.02	−.05	.23	.27	.18	.07
SD
Total sleep duration	.21	.10	.15	−.29	.01	.17	.32
Sleep latency	−.17	.03	−.42*	−.12	−.06	−.11	−.29
Sleep minutes	.22	.03	.25	−.16	.14	.34	.50**
Wake after sleep onset	−.32	−.04	.26	−.02	.25	.11	.25
Mean wake episodes	−.14	.18	−.10	−.21	−.03	.07	.13
Sleep efficiency	−.39*	.04	.28	−.04	.33	.17	.36†
Activity mean	−.35†	.16	−.14	−.01	.11	−.11	.17
Activity index	−.42*	−.07	−.13	.24	.43*	.10	.24
Sleep fragmentation index	−.42*	.29	.02	.12	.27	.30	−.01
Age	.37†	−.07	−.01	.33	−.11	.26	.21
Gender	−.02	.06	.17	.09	.12	.33	.29

Note. Significant or marginal correlations are reported in bold characters. Gender (0 = boys, 1 = girls).

†

p < .10. *p < .05. **p < .01.

Relatively to the standard deviations of actigraphic sleep parameters, findings revealed negative associations between HA and sleep efficiency, activity index, sleep fragmentation index, and activity mean (although the latter association was marginally significant). In addition, RD was negatively correlated with sleep latency, whereas SD was positively related to activity index. Finally, we found that in ADHD preschoolers, ST was positively associated with sleep minutes and sleep efficiency (this last was marginally significant).

Correlations Between Temperament and Character Dimensions and Sleep Questionnaire in the ADHD Group

Correlational analyses between temperamental dimensions and sleep questionnaire in ADHD preschoolers are reported in Table 3. Our results revealed that children who woke up more than twice per night or that took more than 30 min to fall asleep obtained lower scores in the HA temperamental dimension. Children who refuse to fall asleep or that woke from sleep screaming or confused were perceived as more novelty seeker. We also found that children who displayed early morning awakenings were perceived as less RD and that children who sweated excessively while falling asleep or during the night were perceived as less SD. In addition, children who woke up in the morning feeling tired received lower scores in the CO character dimension. Finally, children with difficulty falling asleep, who woke from sleep screaming or confused, and who fall asleep while playing obtained higher scores for ST, whereas those children who sleepwalking were perceived as less ST.

Table 3.

Bivariate Correlations Between Sleep Questionnaire and Temperamental Characteristics in Children With ADHD.

	Harm avoidance (HA)	Novelty seeking (NS)	Reward dependence (RD)	Persistence (PS)	Self-directness (SD)	Cooperativeness (CO)	Self-Transcendence (ST)
Sleep latency > 30 min	−.37†	.03	.08	.23	.20	−.07	.24
Difficulty getting to sleep at night	−.30	.19	.27	−.01	−.04	−.10	.41†
Refuse to fall asleep, cries	−.29	.48*	−.01	−.01	−.01	−.36	.21
Herbal infuse, phytotherapy, or drugs to fall asleep	—	—	—	—	—	—	—
Hypnic jerks	.34	.04	.15	.18	−.09	.07	.16
Rhythmic movement disorders while falling asleep	—	—	—	—	—	—	—
Falling asleep sweating	.20	−.07	.10	−.22	−.38†	.11	−.19
Sleeptalking	−.04	.06	.34	−.15	−.26	.03	.04
Difficulty to fall asleep after night awakenings	−.28	−.19	.24	−.34	−.10	.10	−.05
Nocturnal hyperactivity	−.04	.17	.09	.28	−.06	−.12	−.07
Sleepwalking	.03	−.34	.28	−.16	−.07	.24	−.42*
Difficulty in breathing	−.22	.16	.01	−.03	.23	.11	.24
Sleep apnea	.11	.07	−.05	.22	.13	.01	−.02
Snoring	−.03	−.20	.11	.15	.24	.36	.23
Bruxism	.16	.06	.25	.08	−.05	.06	−.12
Sleep terrors	−.19	.44*	.29	.12	.01	−.22	.47*
Night awakenings > 2	−.49*	.10	.27	−.19	.05	−.10	.12
Nightmares	−.15	.19	−.04	−.02	−.19	−.15	.01
Feeling tired at morning awakening	.03	.33	−.08	.18	−.27	−.37†	.12
Bad mood	−.20	.32	.26	.04	.25	−.16	.24
Early morning awakenings	−.35	−.04	−.38†	−.09	−.02	−.09	−.11
Daytime somnolence	−.01	.11	−.24	−.08	−.23	−.35	−.09
Falling asleep while playing	−.28	.35	.12	.06	.15	−.17	.39†
Falling asleep in inappropriate situations	−.16	.32	−.09	−.04	−.13	−.23	.21

Note. The items of sleep questionnaires were coded as 0 (absence) or 1 (presence) of the behavior. Significant or marginal correlations are reported in bold characters.

†

p < .10. *p < .05.

Discussion

Temperament and Character Profiles in ADHD Versus TD Children

In our study, we found that ADHD children showed a temperamental profile characterized by higher NS, lower PS, SD, CO, and HA when compared with TD children, in agreement with a previous study (Melegari et al., 2015). The study of temperamental profiles with the same instrument (TCI), conducted in school-aged children, confirms our findings. Cho et al. (2008) reported higher NS scores and lower SD scores in ADHD children than in healthy subjects. Similarly, Yoo et al. (2006) have shown that ADHD patients have higher NS levels than control subjects. Furthermore, a recent study revealed that ADHD schoolchildren displayed higher scores in NS and lower scores in PS, SD, and CO compared with children without a diagnosis of ADHD (Donfrancesco et al., 2015). Another study in college students reported that ADHD showed a profile with higher NS and HA and lower PS, SD, and CO levels compared with the control group (Park, Suh, Lee, & Lee, 2016). Our findings, in agreement with the above studies conducted in subjects with different age, confirm that the temperamental profile of ADHD is relatively stable during the lifetime.

Based on the Cloninger’s model, subjects with high levels of NS are depicted as impulsive, explorative, excitable, fickle, quick-tempered and disorderly, intolerant to frustration and rules, and with a tendency to exceed one’s capacity (Cloninger, 1987). These traits are reinforced by poor inhibitory modulatory influences due to low HA. Lower scores on PS indicate a concurrent poor tendency to maintain behaviors that require effortful control to achieve a goal, without continuous social reinforcement. Finally, low scores on SD and CO, respectively, indicate a low ability of children in regulating their behavior in relation to social rules and goals, coping with social-life experiences, and adhering to the rules of a group (Cloninger, 1987).

Relation Between Temperament and Character Dimensions and Objective–Subjective Sleep Parameters in Preschoolers With ADHD

In the present study, HA resulted to be the temperamental dimension best correlated with the several actigraphic parameters. Precisely, lower scores on HA are associated to an increase in activity and awakenings during sleep, to more fragmentation and a decrease in sleep efficiency and sleep duration. Low HA is, also, associated to a higher variability in several of these variables. In addition, higher scores on NS were related to a decrease in total sleep duration and higher scores on RD were associated to a decrease of mean wake episodes and variability in sleep latency.

To our knowledge, the only study attempting to correlate sleeping habits with temperament using the same temperament instrument Junior Temperament and Character Inventory (JTCI) was conducted in TD preschool children and used parent’s sleep report (Chung, Park, An, Kim, & Kim, 2013). This research showed that, similarly to our study, HA was the only temperamental dimension correlated with sleep problems; however, they found that high levels of HA were associated with sleep variables, contrarily to what was expected.

We found a partial agreement between our data and those reported by Molfese et al. (2015) on TD toddlers. These authors reported that toddlers with higher ratings for activity level (component of NS) had less actigraph-recorded nighttime sleep (in agreement with our findings that NS was correlated with a decreased sleep duration), and toddlers with higher soothability ratings (component of RD) had more actigraph-recorded total sleep (in agreement with our findings that higher RD was correlated with less mean wake episodes). Finally, higher scores on the fear (component of HA) were associated with more variability in actigraph-recorded sleep onset time in disagreement with our findings in which higher HA was associated with lower variability in sleep parameters.

The differences found with these studies might be related to the different samples analyzed; our clinical sample had a well-defined and stable profile, the opposite of the extreme individual variability of temperament profiles usually found in TD population.

Similarly to Chung et al. (2013), we also found that HA was the temperamental dimension with a higher number of correlations with sleep. A subject with low HA is characterized by the natural tendency to be exuberant, daring, and disrespectful for exposing himself to danger, and these behaviors might determine a more disrupted sleep.

Some studies have shown that sleep deprivation or sleep disruption in children increase inattention, impulsivity, and lower self-HA behaviors determining an injury proneness (Owens, Fernando, & Mc Guinn, 2005; Valent, Brusaferro, & Barbone, 2001). Furthermore, preschoolers with behavioral dyscontrol, such as hyperactivity, increased emotional reactivity, and decreased attention span temperament related, report a history of more frequent accidents (Jaquess & Finney, 1994; Manheimer & Mellinger, 1967).

Our findings also reveal a strong correlation between character dimensions and sleep parameters. Children with higher scores on SD and ST show, respectively, higher variability in activity index and sleep minutes. The relation between these two character dimensions and sleep problems is partially supported by a study on adult patients with restless legs syndrome (RLS; Altunayoglu Cakmak et al., 2014) that highlighted a negative relation between SD and symptoms of RLS such as “need to move extremities.” In our study, we found that SD is positively correlated with the variability of the activity index. Since in preschool age motor activity is considered to be a typical behavior, it is possible that parents perceive the child activity as an index of self-confidence and autonomy, differently by inhibited children (Eisenberg et al., 2001).

The association of sleep variables and PsTCI dimensions is corroborated by the parental sleep questionnaires, where children perceived to have low HA fall asleep late and interrupt sleep with frequent awakenings while children perceived to be low on RD show a tendency to wake-up early in the morning. Children with higher scores on NS and with lower scores on ST, SD, and CO character traits show, respectively, resistance at bedtime, parasomnias, sweats, and higher tiredness in the morning.

Our results concur with the conclusion that a defined temperament and character profile may be associated with several objective–subjective alterations of sleep parameters and allow us to speculate a bidirectional influence with temperament affecting sleep and daytime behaviors, and with sleep problems affecting behavior of children, thus increasing the influences of temperamental traits.

Neurobiological substrates of Temperament and Sleep

Several studies have reported that temperament and sleep share common neurotransmitter substrates that may account for the strict relation between them. Based on the model by Cloninger (1987), the four temperament dimensions are associated with brain dopaminergic (NS), serotonergic (HA), noradrenergic (RD), and glutaminergic (PS) activity.

The most important neurotransmitters involved in sleep regulation are dopamine and serotonin. Interesting studies confirmed that the association between neurobiological mechanisms underpinning ADHD psychopathology and those of sleep regulation can be due to shared common dopamine and serotonin disfunction (Kirov & Brand, 2014).

Extensive data support that dopaminergic dysfunction plays a central role in the pathophysiology of ADHD (Faraone, Bonvicini, & Scassellati, 2014; Gold, Blum, Oscar-Berman, & Braverman, 2014) as well as of other sleep disturbances, such as RLS. Children with ADHD have high NS and a high level of activity during sleep; however, the actigraphic sleep parameters of activity correlates with HA and not with NS.

The link between HA and variation in the serotonin transporter gene (5-HTTLPR; Bouvette-Turcot et al., 2015; Mazzanti et al., 1998) and the correlation of HA with several sleep parameters support the fact that serotonin (5-HT) is one of the most important neurotransmitters involved in the regulation of sleep and temperament. Some studies have indicated that the relationship between serotonin and HA is not direct and that the HA dimension may be correlated with the balance of a complex neurotransmitter network including dopamine (Kim et al., 2011; Yasuno et al., 2001). Serotonin would act through several serotonin receptor subtypes, to either facilitate or inhibit dopaminergic activity (Alex & Pehek, 2007). On the contrary, dopaminergic neurotransmission plays a role in regulating neuronal activity associated with HA (Cloninger, Svrakic, & Przybeck, 1993; Kim et al., 2011; Yasuno et al., 2001) and a significant interaction between two dopamine receptor D4DR, D3DR polymorphisms and the serotonin polymorphism 2-HT2C is found also on other dimensions, such as RD (Ebstein et al., 1997; Kuhn et al., 1999).

These studies support the conclusion that sleep behavior and temperament could be influenced by specific shared neurotransmitter receptor subtypes and that the relationship between ADHD and sleep is the result of the altered modulation of neurotransmitters where temperament might represent the intermediate endophenotype (Kirov & Brand, 2014; Sizoo, van der Gaag, & van den Brink, 2015).

The present study has some limitations that must be acknowledged. Although we considered a clinical sample of ADHD children, we analyzed a small number of subjects; therefore, this study should be considered to be a first exploratory step for future analysis. A further limitation is that we included children with different subtypes of ADHD and different severity symptoms. It is possible that a better selection and detection of subgroups might pick up a more defined correlation between sleep and PsTCI configurations. Finally, our cross-sectional study allows to hypothesize a bidirectional relation between temperament and character dimensions and sleep problems that should be confirmed by longitudinal studies.

Conclusion

Our study is the first that reports a relation between temperament and sleep in preschool children with ADHD using the PsTCI. In agreement with other studies, our findings testify that several temperament and character dimensions are linked to sleep problems as well as to dysregulated daytime behaviors in ADHD children.

In addition, we support the importance of studying complex neurobiological network underlying temperament and character dimensions and sleep, to better understand the mechanisms and the pathophysiological links. Furthermore, this study might have implications for the diagnostic assessment and might give indications on strategies and routines to adopt for children with ADHD and sleep disorders.

Footnotes

Declaration of Conflicting Interests

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: This was not an industry-supported study. This work was performed at the Department of Social and Developmental Psychology, Sapienza University, Rome, Italy, in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Author Biographies

Maria Grazia Melegari is child and adolescent neuropsychiatrist with special expertise in psychiatric and neurodevelopmental disorders in preschool age children. She was clinical director of ADHD Center and Coordinator of Autism Center in “La Scarpetta ASL RM/A” Rome. She is affiliated and scientific collaborator with Department of Developmental and Social Psychology “Sapienza” University, Rome. Her research interests focus on ADHD, temperament, emotional disorders, as well as child and adolescent psychopharmacology; in this filed she has authored several peer-reviewed papers, books and book-chapters

Stefania Sette is a clinical psychologist; after graduating with honors from the Faculty of Medicine and Psychology of Sapienza University, received her PhD at Sapienza University and graduate school in cognitive behavioral psychotherapy. During her doctorate, she had the opportunity to refine his studies at Arizona State University (USA). In 2012 she also received the AIP “young researchers” award. She is currently research fellow at the Department of Developmental and Social Psychology (Sapienza Univ., Rome). Her main research activity concerns the role of individual components (emotional competence, temperamental characteristics) and interpersonal factors in the socio-emotional adaptation of children and adolescents and recently she approached the field of sleep research in infants and children

Elena Vittori is child and adolescent neuropsychiatrist at Center for Research and Treatment of language disorders (Ricerca e Cura Balbuzie e disturbi del linguaggio e dell’apprendimento), Rome and Honorary Judge at the Juvenile Court of Rome. Her main research interests focus on the neuropsychology of developmental disorders (ADHD and autism) and on sleep disorders in children and adolescents with neurodevelopmental disabilities and she is author of several international publications on these topics

Luca Mallia is a senior researcher at the Department of Movement, Human and Health Sciences-University of Rome “Foro Italico”. He earned his PhD degree at the Sapienza-University of Rome in 2007. His research interests are focused on the analysis of the belief systems and decision making processes underpinning risky behaviors in young people. He participated to international research programs, he was coauthor of several international publications, and received scientific awards.

Alessandra Devoto is a clinical psychologist with PhD in cognitive psychology and board certified in Sleep Medicine by the Italian Association of Sleep Medicine (AIMS) with expertise in Cognitive-behavioral treatment of insomnia. She is senior lecturer at the Faculty of Psychology and Medicine at the University of Rome “Sapienza”. Her research interest focus on psychophysiology of sleep-wake cycle and she is author of numerous scientific publications in the field of psychological care of sleep disorders.

Fabio Lucidi, PhD, is a full professor in Psychometrics at the Department of Development and Social Psychology, Faculty of Medicine and Psychology, Sapienza - University of Rome. He has authored over 150 publications mainly in high impact international journals. He is member of the editorial board of Italian Journal of Psychology and of The Open Ergonomics Journal and is an Academic Editor for Plos One. He is the president of the Italian Association of Psychology.

Raffaele Ferri is chief of the Sleep Research Centre and chairs the Unit of Neurology of the Oasi Institute for Research on Mental Retardation and Brain Aging in Troina (Italy), Dr. Ferri specific areas of interest cover the description, analysis and understanding of various aspects of human sleep and sleep disorders. He has published over 300 papers in international peer-reviewed scientific journals, in addition to book chapters and abstracts. He is the currently the president of the Italian Association of Sleep Medicine (AIMS) and vice president of the European Restless Legs Syndrome Study Group; he is an associate editor for the journal Sleep, International Journal of Psychophysiology, PlosONE, and is member of the editorial board of Clinical Neurophysiology, Sleep Medicine, and Sleep Medicine Reviews.

Oliviero Bruni is currently associate professor in Child Neurology and Psychiatry in the Dept. of Developmental and Social Psychology, Sapienza University, Rome. He is founder and past-president of the International Pediatric Sleep Association, member of the Board of Directors of the Italian Association of Sleep Medicine, Field Editor (Pediatrics) of the journal Sleep Medicine and was Chair of the Childhood Sleep Disorders and Development Section of the American Academy of Sleep Medicine (AASM). He published over 170 peer-reviewed scientific papers, in addition to several monographs and book chapters.

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